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Like father like son
A fresh review of the inheritance of acquired characteristics
Yongsheng Liu
T
he natural environment is in a state
of constant flux and living organisms
are perpetually challenged to adapt
to these changes. Yet the mechanisms of
adaptation, which lead to the development
of new characteristics or behaviours, have
troubled philosophers and scientists since
the days of ancient Greece. In fact, it was not
until 1859, when Charles Darwin (1809–
1882) published The Origin of Species
that part of the puzzle was solved. Darwin
developed his theory of natural selection to
explain the enormous diversity and adaptability of living organisms. He theorized
that organisms of the same species develop
subtle differences in their phenotypes that
make them more or less able to survive
and reproduce, and that those differences,
which improve survival and reproduction,
are passed on to future generations.
…despite its success, Darwin came
to regard The Origin of Species as
an incomplete explanation of his
theory of evolution
But Darwin did not address the question of how the variety, on which natural
selection acts, arises in the first place. This
piece of the puzzle was supplied seven
years later, in 1866, when Gregor Mendel
(1822–1884) published his laws of inheritance. Mendel provided a mathematical
model that explained how the phenotype
of an organism is dependant on its genotype, and that genotypes are passed on from
parents to their progeny and recombine to
create new variations. It was later, in 1953,
that Darwin’s and Mendel’s explanations
were fully completed, when Francis Crick
and James Watson published the structure
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of DNA, which explained the mechanism of
how genes are copied and inherited.
Yet, despite its success, Darwin came to
regard The Origin of Species as an incomplete explanation of his theory of evolution
(Darwin, 1859). Later in his career, he spent
considerable time studying the underlying
causes of the variations that he believed
were subject to natural selection and the
laws of inheritance. He published his
insights in a two-volume book, The Variation
of Animals and Plants under Domestication
(Darwin, 1868), in which he developed
his ‘provisional hypothesis of pangenesis’.
This theory attempted to explain how the
changes in the physiology of an organism
resulting from its environment—so-called,
acquired characteristics—could also be
passed on to its progeny, even without
genetic information encoding them. In
addition, it would also explain many other
observations pertaining to variation, heredity and development. However, although
the scientific community widely accepted
Darwin’s theory of natural selection and its
explanation of evolution, his theory of pangenesis was largely regarded as wrong and
ignored by geneticists.
Even now, more than a century after
Darwin’s death, whether phenotypes that
are not encoded in the genome can be
transmitted across generations, and how this
is possible, still remain unanswered questions. Furthermore, if the inheritance of such
acquired characteristics occurs at all, does it
play a significant role in evolution?
T
his question has been the subject
of heated controversy for more
than 2,000 years and has attracted
renowned scientists and philosophers to both
sides of the debate. Rather anecdotally, one
of the earliest proponents was Hippocrates
of Cos II (ca. 460–370 BC), ‘the father of
medicine’, who firmly believed in the inheritance of acquired characteristics, based on
his observations of the somewhat mythical
race of people, the Macrocephali. He wrote
of their elongated heads: “The characteristic
was thus acquired at first by artificial means,
but, as time passed, it became an inherited
characteristic and the practice was no longer
necessary” (Adams, 1891).
…if the inheritance of such
acquired characteristics occurs at
all, does it play a significant role
in evolution?
More famously, Jean-Baptiste Lamarck
(1744–1829), who coined the term ‘biology’,
devoted a chapter of his book, Philosophie
Zoologique, published in 1809, to the influence of the environment on the activities and
habits of animals. He wrote that environmental changes in “situation of climate, food,
habits of life, etc., lead to corresponding
changes in animals and plants in size, shape,
proportion of parts, color, consistency, swiftness and skill”, which can be passed on to
the next generation (Lamarck, 1809).
Indeed, Darwin also linked the cause of
some variation with changes in the environ­
ment. He favoured the view that “variations of all kinds and degrees are directly or
indirectly caused by the conditions of life
to which each being, and more especially
its ancestors, have been exposed […] if it
were possible to expose all the individuals of a species during many generations to
absolutely uniform conditions of life, there
would be no variability” (Darwin, 1868).
However, various early attempts to provide scientifically satisfying proof for the
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inheritance of acquired characteristics all
failed. Most geneticists eventually took the
view that characteristics acquired as a result
of environmental influences are rarely inherited and that any exceptions to this are of little importance, either for understanding the
mechanisms of evolution or for commercial
breeders to consider in their pedigrees.
An example of this stance was Darwin’s
contemporary, August Weismann (1834–
1914), who was one of the most influential
evolutionary theorists during the nineteenth
century. He entirely rejected the idea of the
inheritance of acquired characteristics and
instead explained heredity by his theory of
the “continuity of the germ plasm”. He held
that, from the very first cell divisions of the
growing embryo, the so-called germ plasm
was destined to become the cells that would
later be passed on during sexual reproduction. Furthermore, he argued, this germ
plasm would remain completely unaffected
by the somatoplasm or environmental influences and would be a ‘safe’ copy of the
embryo’s original genome. In an effort to
disprove the idea of inheritable acquired
characteristics, Weismann cut off the tails of
male and female mice after birth to show
that, even over many generations, tail chopping never produced tailless progeny
(Weismann, 1889).
Most geneticists eventually took
the view that characteristics
acquired as a result of
environmental influences are
rarely inherited, and that any
exceptions to this are of little
importance…
However, critics pointed out that this
experiment did not actually test the inheritance of acquired characteristics because
cutting off a mouse’s tail is an external
modification. In fact, Lamarck distinguished
between two types of acquired characteristics: directly acquired, such as removal of
the tail; and indirectly acquired, in response
to a change of habit or environment. In his
view, only indirectly acquired characteristics
could be passed on to progeny (Steele et al,
1998). Darwin made this same distinction:
“a part or organ may be removed during several successive generations, and if the operation be not followed by disease, the lost part
reappears in the offspring” (Darwin, 1868).
T
hus the question remains unanswered:
does the inheritance of acquired characteristics occur? As Otto Landman
(1993) has pointed out, the inheritance of
acquired characteristics is not often encountered in natural science, despite a substantial body of evidence—mostly in bacteria
and other lower organisms—to support it.
This evidence has been accumulated over
the past 2,000 years, but most significantly,
rigorous scientific evidence has replaced
anecdotal evidence during the past century,
resulting in a compelling case for reassessing
the possibility of acquired inheritance.
By way of example, in 1964, Tchang TsoRun and co-workers generated an artificial
hypotrich doublet in the ciliate Stylonychia
mytilus (Tchang et al, 1964). They isolated
a fused macronucleus and some cytoplasm
when the ciliate began to divide asexually,
and the isolated piece developed into mirrorimage doublets with the two ventral surfaces
on the same plane, rather than the usual
back-to-back configuration. These artificial
doublets had a complete set of physiological
and reproductive functions, and were heritable in the normal manner—that is, their progeny had the same phenotype. Using similar
methods, Gray Grimes et al (1980) obtained
the same result in Pleurotricha lanceolata.
In the 1950s, Pyotr Sopikov (1903–1977)
claimed to have induced inheritable acquired
characteristics in birds by performing
repeated blood transfusion from black
Australorp hens to White Leghorn hens. He
found that the subsequent mating of the
White Leghorn hens with White Leghorn
roosters yielded progeny with a modified
phenotype (Sopikov, 1954). Importantly, other
researchers between 1950 and 1970 confirmed Sopikov’s observations. For example,
Maurice Stroun and co-workers reported that
birds of the White Leghorn variety, which were
repeatedly injected with blood from the gray
guinea fowl, produced progeny with some
gray or black-flecked feathers in the second
and later generations (Stroun et al 1963).
There are also many records of graftinduced inheritable changes in plants and
Darwin was the first to compile the available
information on graft hybrid individuals produced from the cellular tissue of two different
plants (Darwin 1868). Several famous plant
breeders, including Luther Burbank (1849–
1926) and Ivan Michurin (1855–1935), created plants with inheritable characteristics
that were acquired from the tissues of both
original plants. In addition, about 500 papers
on these types of hybridization experiment
©2007 European Molecular Biology Organization
were published in the Soviet Union during the 1950s, although Western geneticists
largely ignored the literature and dismissed
the work as based on fraudulent results. Over
the past decades, however, independent
scientists have repeatedly shown that graftinduced variant characteristics in plants are
stable and inheritable (Liu, 2006a).
In addition to physical phenotypes,
behavioural characteristics also appear to be
inheritable. Swedish scientists recently produced substantial evidence when they raised
Red junglefowl—the ancestors of modern
chickens—and domesticated White Leghorn
chickens in a stressful environment. They
exposed the birds to an unpredictable rhythm
of darkness and light that reduced their ability to solve a spatial learning task (Lindqvist
et al, 2007). The progeny of stressed White
Leghorn—but not Jungle Fowl—birds, raised
without parental contact, had a reduced spatial learning ability compared with the progeny of non-stressed birds in a similar test. The
progeny of the stressed White Leghorns were
also more competitive and grew faster than
the progeny of non-stressed parents, suggesting that behavioural stress responses were
transmitted to the next generation.
T
he inheritance of acquired characteristics is not limited to physical and
behavioural traits. In 1980, Gorczynski
and Steele provided evidence that the inheritance of acquired characteristics plays a
role in the developing immune system. They
showed that neonatally acquired antigenspecific immune tolerance to foreign H-2
antigens in male mice is transmitted to a
high proportion (50–60%) of first-generation
offspring. Further incrossing and outcrossing
of these first-generation mice showed that
20–40% of second-generation animals were
again specifically tolerant or hyporesponders to the original H-2 antigen (Gorczynski
& Steele, 1980). Several attempts to repeat
these experiments yielded both positive and
negative results, and produced a heated scientific controversy. Just two decades later,
Hilmar Lemke et al (2004) suggested that the
functional impact of maternally acquired IgG
in the newborn is an example of non-genetic
inheritance, and reveals a Lamarckian
dimension to the immune system.
There is also evidence for the inheritance
of non-Mendelian traits in humans. During
the winter of 1945/46, there was a major
famine in much of Europe caused by the
devastation of the Second World War. Many
pregnant women received less than 1,000
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Control
Parental generation (White leghorn layers, domesticated chicken)
Stressed*
Spatial learning
abilities are reduced
in comparison with
the control group.
*Stressed: Chicken under chronic mild stressful treatment (unpredictable light-dark rhythm)
Control**
Offspring (White leghorn layers, domesticated chicken)
Stressed
parents**
Spatial learning
abilities are reduced
in comparison with
the control group.
**Hatched offspring had no contact with the parental generation
Offspring (Red jungle fowl, ancestors of all domesticated chicken)
Stressed
parents**
Spatial learning abilities are NOT reduced
in comparison with
the control group.
**Hatched offspring had no contact with the parental generation
Illustration based on findings by Lindqvist et al, 2007.
calories per day during the last trimester of
their pregnancy. Researchers Ursula Kyle and
Claude Pichard (2006) found that there was a
clear correlation between the birth weight of
these women’s babies and maternal weight
at parturition, in addition to other physiological and pathological changes in the next
generation. In the Netherlands, researchers
went further and examined the phenotypes
of the next generation—who grew up with
no food restrictions—and found a lingering
relation between a mother’s weight at her
birth and the birth weights of her children
(Susser & Stein, 1994).
Similarly, Andreas Plagemann and colleagues showed that children of overweight or
diabetic mothers have a higher risk of developing high blood pressure and diabetes later
in life (Harder et al, 2001a). They explained
this effect by suggesting that the body’s
‘default’ levels of insulin and other hormones
are ‘set’ during fetal and neonatal development; throughout life, the body’s metabolism
then tries to maintain or restore these ‘set’
levels (Harder et al, 2001b). However, if this
process is disturbed during the early stages of
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development through environmental influences—if the mother has abnormal hormone
levels caused by diabetes or obesity—then the
child’s ‘default’ levels will be set outside the
normal range, with ensuing consequences for
the overall metabolism and disease risk.
I
n summary, there is an increasing body
of evidence for the inheritability of environmentally induced acquired characteristics; however, the problem that has
historically hindered the acceptance of this
theory is the lack of a theoretical framework
to explain the mechanism by which acquired
traits could be inherited. Although Lamarck
took the inheritance of acquired characteristics for granted, he made no attempt to show
how such transmission works. Conversely,
Darwin theorized that the mechanism was
through minute particles or molecules—that
he called ‘gemmules’—which, he proposed,
are expelled by cells that have changed in
response their environment. These gemmules
could then circulate the body and cause other
cells to undergo similar changes—including
cells of the germline.
A modern version of Darwin’s pangenesis is the ‘somatic selection’ hypothesis,
which explains how mutant somatic information could be integrated into the germline. According to the theory, endogenous
retroviral vectors would capture RNA
from somatic cells and transduce them
into germline cells. Once inside, the passenger RNA would be reverse-transcribed
and spliced into the genome of the cell by
recombination (Steele et al, 1998). In addition, Darwin’s theoretical gemmules could
in fact be circulating DNA, prions, mobile
elements or as yet unknown molecules
(Liu, 2006b). What seems clear, however, is
that there might be multiple vectors for the
transmission of environmentally induced
changes to the progeny of an organism.
For example, environmentally induced
genomic rearrangements might be enacted by
transposable elements. Barbara McClintock
(1902–1992), who received the 1983 Nobel
Prize in Physiology or Medicine for the discovery of transposons, was convinced that
environmental stressors could trigger inheritable changes in the genome: “I believe there
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is little reason to question the presence of
innate systems that are able to restructure a
genome. It is now necessary to learn of these
systems and to determine why many of them
are quiescent and remain so over very long
periods of time only to be triggered into
action by forms of stress, the consequences
of which vary according to the nature of the
challenge to be met” (McClintock, 1978).
There is sufficient evidence that this is
at least the case in plants. Various research
groups have shown that specific concentrations of certain mineral nutrients or temperature can cause plants to grow differently.
These phenotypic changes are transmitted
to the progeny and remain stable for several generations (Durrent, 1962). The DNA
modifications associated with these environmentally induced changes have been
extensively characterized (Cullis, 2005).
…observations of the
inheritance of acquired
characteristics are increasingly
compatible with current
concepts in molecular biology
For example, Gerhard Ries et al (2000)
reported that UV-B radiation induces DNA
rearrangements in Arabidopsis thaliana and
tobacco plants, and that the effects of UV-B
on genomic stability increased with each generation, suggesting that there were inheritable
changes occurring in the expression of genes
involved in DNA metabolism. Similarly, Jean
Molinier et al (2006) showed that Arabidopsis
plants treated with short-wavelength radiation
or flagellin had increased somatic homologous recombination of a transgenic reporter.
Furthermore, these increased levels of recombination persisted in subsequent, untreated
generations. The authors concluded from
their study that environmental factors led to
increased genomic flexibility even in successive, untreated generations, perhaps as a
mechanism to increase the potential of the
plants to adapt to changes in environment.
D
uring the past years, the scientific
community has realized that prions—proteins that had already overthrown another scientific dogma: that only
DNA-carrying particles can be infectious
agents—are able to transmit phenotypic information. Susan Lindquist’s work on the yeast
prion sup35 revealed that the protein acts as a
switch so that when the environmental
conditions deteriorate sup35 switches to its
prion state [PS1+], in which translation fidelity is decreased and the ribosome reads
beyond nonsense codons. This in turn allows
the expression of formerly silent genes and
gene variants to create new phenotypes.
[PS1+] is passed on to daughter cells where it
self-replicates by imposing its conformation
on normal sup35 proteins (Shorter &
Lindquist, 2005). In an earlier paper, Yury
Chernoff (2001) had postulated that prions
could be a mechanism for the inheritance of
acquired characteristics. Peter Maury (2006)
has also proposed a mechanism by which
prions store and transmit acquired information in specific β-sheet protein conformations.
These can act as cytoplasmic molecular mem­
ories and can be transmitted to future generations utilizing their self-perpetuating potential.
Another possible mechanism that has
drawn increasing attention in the past few
years is epigenesis. Conrad Hal Waddington
(1905–1975), who first defined ‘epigenetics’ as “…the interactions of genes with their
environment which bring the phenotype into
being” (Waddington, 1942), was a keen supporter of the inheritance of acquired characteristics. It seems that Waddington might have
been right: Lindqvist et al (2007) concluded,
from their experiments with chickens, that
epigenetic modifications might be the mechanism of transmission of stress and physiologi­
cal responses to the next generation. More
generally, epigenetic mechanisms mediate
a semi-independent non-Mendelian inheritance system, which enables environmentally
induced phenotypes to be transmitted to the
next generations ( Jablonka & Lamb, 1998).
Experimental evidence for this comes
from studies using mice. A maternal diet
that supplements methyl-donors with folic
acid, vitamin B12, choline and betaine,
alters the fur colour of their progeny towards
the brown pseudoagouti phenotype (Wolff
et al, 1998; Waterland & Jirtle, 2003). This
diet-induced change in colour distribution
was shown to result from an increase in
DNA methylation at sites in the upstream
intracisternal A-particle transposable element (Waterland & Jirtle, 2003). Therefore,
the effect of a mother’s diet during pregnancy on the phenotype of her progeny
was directly linked to DNA methylation
(Cropley et al, 2006). Tessa Roseboom et al
(2006) therefore suggested that epigenetic
changes such as imprinting, which take
place before conception, might help to
explain the effects of the Dutch Famine on
the next generation.
©2007 European Molecular Biology Organization
Root Gorelick (2004) went even further
and coined the term neo-Lamarckian medicine to describe the effects of epigenetic
inheritance on diseases. Exposure to certain environmental pollutants can alter the
methylation patterns of regulatory genes.
This not only increases the risk of cancer, by
up-regulating genes controlling cell division
or down-regulating tumor suppressor genes,
but might also underlie many other diseases.
Such epigenetic changes could be inheritable, thus transmitting the increased risk of
disease to future generations even if they are
no longer exposed to the contaminant.
H
orizontal
gene
transfer—the
exchange of genes across mating
barriers—has long been recognized as a major force in evolution, particularly among prokaryotes. However, there is
increasing evidence that horizontal gene
transfer also occurs between higher organisms. Ulfar Bergthorsson et al (2003) showed
that mitochondrial genes are frequently
transferred between distantly related flowering plants with various genomic outcomes,
including gene duplication, the recapture
of genes lost through transfer to the nucleus,
and chimaeras. These results suggest the
existence of a mechanism for unrelated
plants to ‘swap’ DNA. Recently, Jeffrey
Mower et al (2004) described two new
cases of horizontal gene transfer from parasitic flowering plants to their host plants, and
presented phylogenetic and geographic evidence that this occurred as a result of direct
physical contact. Their findings complement
earlier discoveries that genes can be transferred in the opposite direction, from host to
parasite plant (Davis & Wurdack, 2004).
In light of the mounting
evidence, can we continue
to ignore Darwin’s theory of
pangenesis, which provides
a mechanistic explanation of
how environmentally-induced
variations are inherited?
Notably, Ivan Michurin’s basic principle
of plant breeding was to manipulate environmental conditions during the early
developmental stage of a plant to induce
phenotypic changes. He used grafting to
‘improve’ plants, and stated that the younger
the plant the more successful the experiment would be (Michurin, 1949). Recent
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grafting experiments showed that endogenous
mRNAs use the phloem as a long-distance
translocation system (Lucas et al, 2001).
Furthermore, the transport of other macromolecules including proteins and nucleic
acids between plant cells is most promis­
cuous in young, undifferentiated tissues and
becomes more restricted as tissues age (Ueki
& Citovsky, 2005). With the realisation that
mRNA species can move around the plant,
and the ability of retroviruses or retrotransposons to reverse transcribe mRNA into
cDNA, it becomes clear that mechanisms
exist for horizontal gene transfer from stock
to scion—and vice versa—by grafting.
I
n a letter to Moritz Wagner, Darwin
wrote: “In my opinion, the greatest error
which I have committed, has been not
allowing sufficient weight to the direct action
of the environment, for example, food and
climate, independently of natural selection.
When I wrote The Origin, and for some years
afterwards, I could find little good evidence
of the direct action of the environment; now
there is a large body of evidence” (Darwin,
1888). During the past decades, the evidence for the inheritance of acquired characteristics has been increasing in both
quantity and quality, as have the number of
hypotheses to explain the phenomenon at
the molecular level. Consequently, observations of the inheritance of acquired characteristics are increasingly compatible with
current concepts in molecular biology
(Landman, 1991). Although this does not
discredit the important contributions made by
Weismann and Mendel, nor in any way revive
the theories of Lamarck or Lysenko, it nevertheless sheds new light on the inheritance of
acquired characteristics.
There are many precedents where once
widely disregarded theories eventually made
their way into the main body of scientific
knowledge. In the early 1940s, Waddington
coined the term epigenetics, which he
derived from Aristotle’s theory of epigenesis. Until the 1980s, epigenetics was barely
mentioned in the scientific literature, yet was
used abundantly from the 1990s onwards, as
experimental evidence began to support its
existence and importance. Similarly, Stanley
Prusiner’s discovery that prions are infectious
agents was long disregarded by the scientific
community, but is now generally accepted.
In light of the mounting evidence, can
we continue to ignore Darwin’s theory of
pangenesis, which provides a mechanistic explanation of how environmentally
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induced variations are inherited? Do we in
fact need to enrich and expand Darwin’s
pangenesis, and develop a modern theory of
inheritance, which is broader in scope and
consistent with the wealth of experimental
evidence? A wider understanding of how
acquired characteristics are inherited would
not only indicate that there is much more
to inheritance than genes and Mendelian
genetics, but would also create new intellectual challenges and give a wider perspective
of evolution.
As Darwin wrote to Hooker: “You will
think me very self-sufficient, when I declare
that I feel sure if Pangenesis is now stillborn it will, thank God, at some future time
reappear, begotten by some other father,
and christened by some other name. Have
you ever met with any tangible and clear
view of what takes place in generation,
whether by seeds or buds, or how a longlost character can possibly reappear; or
how the male element can possibly affect
the mother plant, or the mother animal, so
that her future progeny are affected? Now
all these points and many others are connected together, whether truly or falsely is
another question, by Pangenesis. You see I
die hard, and stick up for my poor child”
(Darwin, 1988).
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©2007 European Molecular Biology Organization
Yongsheng Liu is at the Henan Institute of Science
and Technology in Xinxiang, China and the
Pangenesis Institute in Edmonton, Canada.
E-mail: [email protected]
doi:10.1038/sj.embor.7401060
EMBO reports VOL 8 | NO 9 | 2007 8 0 3